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The Journal of Membrane Biology

, Volume 78, Issue 3, pp 235–248 | Cite as

Slow potential changes in mammalian muscle fibers during prolonged hyperpolarization: Transport number effects and chloride depletion

  • Peter H. Barry
  • Angela F. Dulhunty
Articles

Summary

Mammalian skeletal muscle fibers exhibit large slow changes in membrane potential when hyperpolarized in standard chloride solutions. These large slow potential changes are radically reduced in low chloride solutions, where the faster and smaller potential change (“creep”), usually observed in amphibian fibers, becomes apparent. The slow potential change during a hyperpolarizing current pulse leads to an increase in apparent resistance of up to nine times the instantaneous value and takes minutes to reach a steady value. It then takes a similar time to decay very slowly back to the resting membrane potential after the current pulse. The halftime for the slow potential change was found to be inversely proportional to the current magnitude. From measurements of immediate postpulse membrane potentials, assuming constant ionic permeabilities, the internal chloride concentration was calculated to decrease exponentially towards a steady value (e.g., for one fiber from 12.3 to 6.6mm after a 330-sec pulse). The time course and magnitude of the concentration change were predicted from chloride transport number differences, and the known and measured properties of the fibers, and were found to agree very well with the values obtained from experimental measurements. In addition, the shapes of theV2-V1 responses, measured in the three-electrode current clamp set-up with either potassium chloride or potassium citrate current electrodes, were as predicted by transport number chloride depletion effects and were at variance with the predictions of a permeability change mechanism.

Key Words

transport number effects chloride depletion slow potential changes slow conductance changes creep mammalian muscle 

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References

  1. Adrian, R.H., Chandler, W.K., Hodgkin, A.L. 1970. Voltage clamp experiments in striated muscle fibers.J. Physiol. (London) 208:607–644Google Scholar
  2. Adrian, R.H., Freygang, W.H. 1962. The potassium and chloride conductance of frog muscle membrane.J. Physiol. (London) 163:61–103Google Scholar
  3. Almers, W. 1972a. Potassium conductance changes in skeletal muscle and the potassium concentration in the transverse tubules.J. Physiol. (London) 225:33–56Google Scholar
  4. Almers, W. 1972b. The decline of potassium permeability during extreme hyperpolarization in frog skeletal muscle.J. Physiol. (London) 225:57–83Google Scholar
  5. Barry, P.H. 1977. Transport number effects in the transverse tubular system and their implications for low frequency impedance measurement of capacitance of skeletal muscle fibers.J. Membrane Biol. 34:383–408CrossRefGoogle Scholar
  6. Barry, P.H. 1983. Effects of unstirred-layers on the movement of ions across cell membranes.Proc. Aust. Physiol. Pharmacol. Soc. 14:152–169Google Scholar
  7. Barry, P.H., Adrian, R.H. 1973. Slow conductance changes due to potassium depletion in the transverse tubules of frog muscle fibers during hyperpolarizing pulses.J. Membrane Biol. 14:243–292CrossRefGoogle Scholar
  8. Barry, P.H., Diamond, J.M. 1984. Effects of unstirred layers on membrane phenomena.Physiol. Rev. (in press) Google Scholar
  9. Barry, P.H., Dulhunty, A.F. 1983. Slow conductance changes in mammalian muscle fibers during prolonged hyperpolarization.Proc. Aust. Physiol. Pharmacol. Soc. 14:41P Google Scholar
  10. Barry, P.H., Hope, A.B. 1969. Electroosmosis in membranes: Effects of unstirred layers and transport numbers. I. Theory.Biophys. J. 9:700–728PubMedGoogle Scholar
  11. Davey, D.F., Dulhunty, A.F., Fatkin, D. 1980. Glycerol treatment in mammalian skeletal muscle.J. Membrane. Biol. 53:223–233CrossRefGoogle Scholar
  12. Dewhurst, D.J. 1960. Concentration polarization in plane membrane-solution systems.Trans. Faraday Soc. 56:599–609CrossRefGoogle Scholar
  13. Dulhunty, A.F. 1978. The dependence of membrane potential on extracellular chloride concentration in mammalian skeletal muscle fibers.J. Physiol. (London) 276:67–82Google Scholar
  14. Dulhunty, A.F. 1979. Distribution of potassium and chloride permeability over the surface and T-tubule membranes of mammalian skeletal muscle.J. Membrane Biol. 45:293–310CrossRefGoogle Scholar
  15. Eisenberg, R.S., Gage, P.W. 1969. Ionic conductances of the surface and transverse tubular system in frog sartorious fibers.J. Gen. Physiol. 53:279–297PubMedGoogle Scholar
  16. Goldman, D. 1943. Potential impedance and rectification in membrane.J. Gen. Physiol. 27:37–60CrossRefGoogle Scholar
  17. Hodgkin, A.L., Katz, B. 1949. The effects of sodium ions on the electrical activity of the giant axon of the squid.J. Physiol. (London) 108:37–77Google Scholar
  18. Hodgkin, A.L., Nakajima, S. 1972. Effect of diameter on the electrical constants of frog skeletal muscle fibers.J. Physiol. (London) 221:105–120Google Scholar
  19. Lipicky, R.J., Bryant, S.H. 1966. Sodium, potassium, and chloride fluxes in intercostal muscle from normal goats and goats with hereditary myotonis.J. Gen. Physiol. 50:89–111PubMedGoogle Scholar
  20. Palade, P.T., Barchi, R.I. 1977. Characteristics of chloride conductance in muscle fibers of rat diaphragm.J. Gen. Physiol. 69:325–342PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1984

Authors and Affiliations

  • Peter H. Barry
    • 1
    • 2
  • Angela F. Dulhunty
    • 1
    • 2
  1. 1.Nerve-Muscle Research Centre, School of Physiology and PharmacologyUniversity of New South WalesKensingtonAustralia
  2. 2.Department of AnatomyUniversity of SydneyAustralia

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